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Learning by Association in Plants Monica Gagliano1, Vladyslav V

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Learning by Association in Plants Monica Gagliano1, Vladyslav V www.nature.com/scientificreports OPEN Learning by Association in Plants Monica Gagliano1, Vladyslav V. Vyazovskiy2, Alexander A. Borbély3, Mavra Grimonprez1 & Martial Depczynski4,5 In complex and ever-changing environments, resources such as food are often scarce and unevenly distributed in space and time. Therefore, utilizing external cues to locate and remember high-quality Received: 26 July 2016 sources allows more efficient foraging, thus increasing chances for survival. Associations between environmental cues and food are readily formed because of the tangible benefits they confer. While Accepted: 08 November 2016 examples of the key role they play in shaping foraging behaviours are widespread in the animal world, Published: 02 December 2016 the possibility that plants are also able to acquire learned associations to guide their foraging behaviour has never been demonstrated. Here we show that this type of learning occurs in the garden pea, Pisum sativum. By using a Y-maze task, we show that the position of a neutral cue, predicting the location of a light source, affected the direction of plant growth. This learned behaviour prevailed over innate phototropism. Notably, learning was successful only when it occurred during the subjective day, suggesting that behavioural performance is regulated by metabolic demands. Our results show that associative learning is an essential component of plant behaviour. We conclude that associative learning represents a universal adaptive mechanism shared by both animals and plants. The ability to choose among different and often conflicting options, and predict outcomes, is a fundamental aspect of life1–4. One form of choice behaviour is based on establishing an association between an occurrence of external events and the opportunity to satisfy internal homeostatic needs, such as hunger, thirst or sleep. The notion that choices are driven by the expectation of their rewarding outcome goes back to Aristotle5 and has been observed extensively across the animal kingdom6–9. However, it remains unknown whether this is also true for plants. In the complex photosynthetic world of plants, light plays an especially important role in growth and survival. Its role is dual. On the one hand, light energy is necessary for processes of biosynthesis. On the other hand, light provides a time cue for entrainment of the circadian rhythm to the 24-h cycle, thereby optimizing the adjustment of growth and metabolism to the seasonal variation of the photoperiod10. Therefore, the ability to detect salient cues that increase efficiency in foraging for light is absolutely essential and confers a significant evolutionary advantage. Plants have recently been found to acquire new behaviours to enhance foraging efficiency for light through the non-associative learning process of habituation11, and thus to facilitate photosynthesis and growth. However, it remained unknown whether plants can also learn through forming associations. To investigate this possibility, we employed a classical conditioning paradigm where a neutral environmental cue (a conditioned stimulus, CS) predicted the occurrence of light, which is biologically significant (an uncondi- tioned stimulus, US). In the first experiment, pea seedlings (n =​ 45) were entrained to an 8-h light:16-h dark cycle for 5–8 days. In the subsequent 3-d training period, they were kept in darkness with the exception of 1-hour light exposures during the three daily training sessions. Training occurred individually inside a Y-maze, where the air- flow produced by a fan ([F] as the CS) and a blue LED light ([L] as the US) were systematically presented accord- ing to a specific protocol (Fig. 1 and details in Methods section; see also Extended Data Fig. 1 and Supplementary Video 1). Prior to training, seedlings were randomly assigned to one of 2 experimental groups. In one group exposure to the light and fan was on the same arm of the maze [F +​ L], whereas in the other group light and fan were on oppo- site arms [F vs L] (Fig. 1Ai,ii). Accordingly, this design tested for both a positive association of the fan (CS) with light (plant trained to seek out fan as a predictor of light) and a negative association of the fan with light (plant trained to avoid the fan and find light on the side of the tube with no air movement). The protocols were main- tained throughout the 3-d training period. However, to render the direction of the incoming light unpredictable, 1Centre for Evolutionary Biology, School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia. 2Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, OX1 3PT, United Kingdom. 3Institute of Pharmacology and Toxicology, University of Zurich, Zurich, 8057, Switzerland. 4Australian Institute of Marine Science, Crawley, WA 6009, Australia. 5Oceans Institute, University of Western Australia, Crawley, WA 6009, Australia. Correspondence and requests for materials should be addressed to M.G. (email: monica. [email protected]) SCIENTIFIC REPORTS | 6:38427 | DOI: 10.1038/srep38427 1 www.nature.com/scientificreports/ Figure 1. Training and testing protocol for associative learning in pea seedlings. (A) During training seedlings were exposed to the fan [F] and light [L] on either the same arm (i) or on the opposite arm (ii) of the Y-maze. The fan served as the conditioned stimulus (CS), light as the unconditioned stimulus (US). During testing with exposure to the fan alone two categories of responses were distinguished. Correct response: Seedlings growing into the arm of the maze where the light was “predicted” by the fan to occur [green arrow; iii (corresponding to scenario i) and iv (corresponding to scenario ii)]; Incorrect response: Seedlings growing into the arm of the maze where the light was not “predicted” by the fan to occur (black arrow; iii and iv). (B) Seedlings received training for three consecutive days before testing. Each training day consisted of three 2-h training sessions separated by 1-h intervals. The 90-min CS preceded the 60-min US by 60 minutes so that there was a 30-min overlap. (i). During the 1-day testing session, seedlings were exposed to the fan alone for three 90-min sessions (ii). Seedlings of the control group were left undisturbed (no fan, no light; iii). its position with respect to the arm of the maze was re-assigned for each 120-min training session (details in Methods section). During training, the seedlings grew and approached the Y-bifurcation of the maze. Before the testing day, the seedlings were further subdivided randomly into a test group (n =​ 26) and a control group (n =​ 19; the numbers are unequal due to a technical problem). The test group was exposed only to the fan during the three 90-min sessions. In this group, to control for the influence of innate phototropic response, the fan was placed in the arm opposite to last light exposure in the [F +​ L] group and on the arm of last light exposure in the [F vs L] group. The seedlings of the control group were left undisturbed. On the morning after the testing day, we visually inspected the seedlings and recorded the arm of the maze they had grown into (Fig. 1Aiii,iv). As expected, we found that all seedlings of the control group grew into the arm of the maze where the blue light had been presented in the last training session (white bars; Fig. 2). This result corroborates the well-known innate phototropic response of seedlings to blue light12. In contrast, in the test group, the majority of seedlings exhibited a conditioned response to the fan (green bars; Fig. 2). In the [F +​ L] group, 62% of the seedlings grew towards the fan (Fig. 2A), whereas in the [F vs L] group, 69% of the seedlings grew in the direction opposite to the fan (Fig. 2B). Thus, the first experiment has shown that plants are able to form associations to enhance foraging success. In animals, the circadian system provides a framework for a wide range of behaviours. The ability to anticipate changes in food availability enables efficient interactions of the organism with the environment in a time of day dependent manner, and facilitates learning13,14. Great progress has been achieved in characterizing the molecular and physiological basis of circadian rhythmicity in plants15. However, it remains unknown whether the time of day modulates behavioural processes such as learning, in plants. In our second experiment, seedlings (n =​ 83) were trained and tested inside a Y-maze, where temperature and light served as Zeitgebers16 (Fig. 1B; details in Methods section). The training and testing procedure corresponded to that of the first experiment. However, exposure to fan and blue light occurred always on the same arm of the maze ([F +​ L] condition). The main variable was the phase of the 24-h temperature cycle in which the training and testing sessions occurred. Prior to training, the seedlings were randomly assigned to one of 3 experimental groups. They were main- tained under controlled environmental conditions (12-h light:12-h dark coinciding with high-low temperature 21 °C:17 °C). The temperature cycle served as the Zeitgeber that was maintained throughout the training and testing periods. The timing of the experimental ‘day’ (light + 21 °C) in the growth chamber varied between the groups (Fig. 3A): Group 1 experienced ‘day’ from 07:00–19:00 (‘Light’), Group 2 from 01:00–13:00 (‘Light-Dark’) and Group 3 from 19:00–07:00 (‘Dark’). After emergence, each seedling was transferred into its individual Y-maze where one of the arms was used to deliver both the unconditioned stimulus (light, US) and the conditioned stim- ulus (fan, CS). Since both [F vs L] and [F +​ L] protocols had been equally effective in the first experiment, only the latter protocol was used here.
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